Vol. 43: 151-159. 1988
MARINE ECOLOGY - PROGRESS SERIES
Mar. Ecol. Prog. Ser.
I
Published March 24
Active emergence of meiofauna from intertidal
sediment
Werner Armonies
Biologische Anstalt Helgoland (Litoralstation),D-2282 List, Federal Republic of Germany
ABSTRACT. Laboratory experiments were conducted to test for active meiofaunal emergence from
intertidal sediment in the absence of currents. Copepoda, Ostracoda, Plathelrninthes and Polychaeta
actively left submerged glass jars containing undisturbed sandy sediment. Ostracoda and juvenile
Bivalvia moved to the sediment surface and climbed out of the glass jars while other taxa left the jars by
swimming. In no case d ~ Nematoda
d
or Ohgochaeta leave the sediment. During a single nocturnal high
tide, 87 % of Copepoda, 67 U/o of Ostracoda and 42 % of Plathelminthes may leave the sediment.
Emigration rates are significantly smaller during diurnal high tides. Copepoda were randomly d ~ s t r i buted in the water column 10 to 50 cm above the bottom and Plathelminthes between 10 and 40 cm
There are specific differences in the emigrahon rates of plathelmlnth taxa. Diatom-feeders, copepodfeeders and unspecific predators emerged In sign~ficantlyhigher proportions than did nematodefeeders and bacteria-feeders. Results suggest high mobility and high transport rates of intertidal
meiofauna above the sediment
INTRODUCTION
Although meiobenthos was traditionally thought to
be strictly infaunal, recent investigations report on
meiofaunal occurrence in the water column (e. g. Alldredge & l n g 1977, 1980, 1985, Porter & Porter 1977,
Hobson & Chess 1979, Hammer 1981, McWilliam et al.
1981, Sibert 1981, Ohlhorst 1982, Youngbluth 1982,
Fancett & l m m e r e r 1985, Hicks 1986, Walters & Bell
1986). Studies on recolonization of experimentally disturbed sediment and short-tern~meiobenthic surveys
often yleld indirect evidence for meiobenthos dispersing via the water column (e. g. Bell & Sherman 1980,
Sherman & Coull 1980, Thistle 1980, Hockin & Ollason
1981, Palmer & Brandt 1981, Chandler & Fleeger 1983,
Fleeger et al. 1984, Kern & Bell 1984). No regular
emergence was found in the studies of Hagerman &
IZleger (1981),Palmer (1984) and Palmer & Gust (1985),
all of which were performed with muddy sediments.
They concluded that the occurrence of meiobenthos in
the water column is a passive process caused by erosion. In contrast most of the studies assuming active
emigration of meiobenthos derived from sandy sediment or seagrass meadows. However, with the exception of Sibert (1981) and Hockin & Ollason (1981) all the
above studies deal with tropical to warm-temperate
Inter-Research/Printed in F R Germany
habitats, and direct evidence for meiobenthos entering
the water column has up to now been restricted to
subtidal areas.
In boreal intertidal and supratidal sand, meiobenthos
performs more or less regular tidal vertical migrations
in the sediment (Meineke & Westheide 1979). When
the sand is disturbed by turbulence in the overlying
water the majority of the fauna responds by downward
migration (Boaden 1968); only various Copepoda and
Plathelminthes move upward (Boaden & Platt 1971).
Downward movement will reduce the risk of being
suspended, and upward migrations will enhance suspension-rates. In muddy sediment, water flow causes
only minor differences in the vertlcal pattern of
meiofauna (Palmer & Molloy 1986) but above-ground
structure (Spartina culms) may enhance copepod
emergence under some hydrodynamical conditions
(Palmer 1986).
The aim of this study was to investigate the rates of
zoobenthos actively emerging from boreal intertidal
sandy sediment. The passive component of meiobenthic occurrence in the water column was experimentally excluded - though not denied. Active emigration
from the sediment may be a means of meiofaunal
dispersal (Gerlach 1977, Alldredge & f i n g 1980, Bell &
Sherman 1980) but may also offer additional prey
152
Mar. Ecol. Prog. Ser. 43: 151-159, 1988
(Decho 1986). On the other hand, meiofauna leaving
the sediment may itself be subject to increased predation (Hobson & Chess 1976, Fulton 1982, Ohlhorst
1982).In many cases it is not known whether predators
on meiofauna catch their prey in the water column, at
the sediment surface, or by burrowing (e. g. Zander &
Hartwig 1982, Sogard 1984).
MATERIAL AND METHODS
Sampling. For all experiments, samples were collected from a 30 X 30 m plot of the Konigshafen
wadden area near the Island of Sylt (North Sea). For a
general description of the area see Reise (1985). The
plot is rather sheltered and the sediment is mainly
composed of medium sand (median diameter of sand
grains 315 pm, sorting coefficient 1.5) with moderate
amounts of detritus (loss on ignition 0.48 %). Experiments were performed between May a n d July 1987.
Seawater temperature in May was 12 "C and
increased to 15 to 16 "C in July. Air temperature varied between 10 and 20°C. The sampled plot is
positioned a t mid-tide level (50 % tidal emersion);
average tidal range is about 1.8 m in this area and
about 0.9 m at the plot.
Sediment samples were collected with glass or plastic tubes to a depth of 2.5 cm. All experiments were
simultaneously conducted in 10 aquaria (10 parallels).
Samples were collected during low tide, about 2 h
before the sample site was again flooded by the sea.
These 2 h were used for transport to the laboratory and
sample preparation. Thus the experimental submersion
started a t the same time as the sample site was flooded
in the field.
Experimental treatments and null hypotheses.
Experiment I: Do meiobenthos actively leave the sediment? Plastic aquaria (24 cm long and 12 cm wide)
were filled with 2 1 of filtered seawater and stored for
24 h to adapt to the experimental temperature of 12 "C
(= actual field temperature). Ten samples of 2 cm2
surface area were collected at each of 5 sites and
transferred into 10 cm3 glass jars. In the laboratory, jars
were cautiously filled with 12 "C filtered seawater without agitating the surface of the samples. Five samples
(one from each site) were subsequently submerged into
each of the 10 aquaria. For the next 4 d, benthos could
emigrate from the sediment and swim or climb into the
aquaria. To record the course of emigration, the jars
were transferred to a second set of aquaria after fixed
periods and the water of the previously used aquaria
poured through 63 urn meshes to retain emigrated
fauna.
With modification of the light regime, the experiment
was repeated 3 times: Expt Ia was performed in con-
tinuous light (50 pE m-2 s-') with water exchange
every 24 h. Expt Ib was performed in continuous darkness except when transferring the glass jars into a new
set of aquaria which was done every 24 h. Finally, Expt
Ic was performed under a 18/6 h day/night rhythm with
water exchange every 6 h.
Expt I tested the following hypotheses:
H, (1): There is no active emigration of benthos from
the sediment - fauna1 abundance in the experimental
aquaria does not significantly differ from zero.
H, (2): Emigration is random in time - the rates of
emigrating fauna do not differ among the 4 d of experimentation.
H, (3): There are no differences in the percentage
emigration rates between taxa - all taxa behave the
same.
Experiment II: Percentage emigration during one
tidal cycle o f submersion. Experimental design was as
Expt I, with 2 exceptions: (1) smaller aquaria were used
(400 cm3 seawater instead of 2000 cm3) and only one
glass jar with sediment was submerged per aquarium;
(2) glass jars containing the sediment were transferred
to a new set of aquaria at l h intervals (total 6 h). The
size of sediment samples was 1 cm2 surface area, sampled to a sediment depth of 2.5 cm. Expt I1 was performed twice: Expt IIa during daytime, with light
(50 pE m-2 S-'), and Expt IIb during night-time, in the
dark. It tested the hypothesis
H, (4): The pattern of emergence is random over time
(6 h).
Experiment III: Distance meiobenthos swims above
bottom. The previous experiments monitored the rate
of benthos leaving the sediment, either swimming or
climbing out of the jars. Expt I11 only recorded actively
swimming benthos and tested the hypothesis H, (5).
There is no difference in the abundance of swimming
benthos between 10 and 50 cm above bottom.
Ten plastic barrels (34 cm in diameter and 57 cm
high) were filled with filtered seawater to a height of
55 cm. As a source of swimming benthos, 3 Petri
dishes containing 60 cm2 X l cm surface sediment
were submerged into each of the barrels. These
dishes were initially filled with filtered seawater to
the rim, any material adhering to the water surface
was removed by slight decantation, the dishes were
again filled with seawater and finally cautiously submerged into the barrels. Five plastic boxes of 500 cm3
volume were submerged into each barrel without
contact to the ground or side walls. There was no
possibility of entering the boxes other than by swimming. The upper rim of the boxes were 10, 20, 30, 40,
and 50 cm above ground, respectively. Boxes were
removed after 6 h storage in the dark and their water
content sieved through 63 pm meshes to retain swimming benthos.
Armonies: Emergence of meiofauna from sediment
Experiment IV: Specific composition of emigrating
a n d non-emigrating Plathelminthes. Fewer species
were recorded as active emigrators in the previous
experiments than are normally found in the sampled
tidal flat. Expt IV checked for specific differences in the
plathelminth emergence pattern. It tests the hypothesis
H, (6): There is no difference in the rates of emigration
between plathelminth species (subordinated taxa,
feeding types).
No extra experiments were performed to check for
this point. Instead, the species con~positionof Plathelminthes emerging in Expt Ib was compared to the
species composition of non-emigrators.
Test of experimental methods. Sediment sampling
causes at least slight mechanical disturbance of the
sediment structure. Meiofaunal behavior might be
influenced by these disturbances, resulting in artifacts
in the experiments outlined above. The effect of
mechanical disturbance on meiofaunal emigration was
tested using experimental designs like Expt I1 on
6 levels of mechanical disturbance:
(1) Sampling tubes were closed at the bottom and
directly used in experiments - no transference into
glass tubes.
(2) 'Normal sampling': cores were sampled with plastic tubes and transferred into glass tubes for transport
and experimentation - slight deformation of the sediment structure.
(3) 'Normal sampling' + mechanical stirring of the
sediment.
(4) 'Normal sampling' + destruction of the sediment
structure by shaking of the glass containers.
(5) 'Normal sampling', but the sediment colun~nwas
turned upside down.
(6) Combination of (3) and (4) to completely destroy
the sediment structure.
With the exception of Plathelminthes which left the
sediment turned upside down a t significantly higher
rates(U-test, p < 0.001) when compared to (1) and (2),
the above treatments did not affect emigration rates in
the previously described experimental design. However, this does not mean that meiobenthos might not
generally be susceptible to this kind of disturbance. To
avoid inadmissible generalization beyond the level of
this study, I will not present any further data. They can
b e obtained on request.
Statistical treatment. In general, abundance data
differ significantly from a normal distribution. Therefore, the non-parametrical U-test (Wilcoxon et al., in
Sachs 1984) is used throughout as a conservative measure. Significant results are indicated by '(p< 0.05),
' ' ( p < 0.01) and ' ' ' (p< 0.001).The standard deviation
given in the tables does not intend to describe the data
distribution but is used to indicate the range of variability.
153
RESULTS
Taxonomic composition of the metazoan benthos at
the sampled plot
Ten sediment samples of 2 cm2 surface area (0 to
2.5 cm layer) were randomly collected at the sample
site (20 June 1987). Grain-by-grain sorting of these
samples (without fixation) yielded an average of 1906
metazoans below 10 cm2 surface area. Nematoda were
most abundant (990 ind. 1 0 c m - ~= 51.8 O/O of metazoan
benthos), followed by Copepoda (520 ind. 1 0 ~ m -=~
27.2 %), Ostracoda (198 ind. ~ O c r n - ~= 10.4 %),
Polychaeta (4.1 %), Oligochaeta (3.5 %), and Plathelminthes (2.7 %). Other taxa, such as Gastrotricha,
Gnathostomulida and Halacarida were present but
together supplied < 1 % of metazoans.
Experiment I: Do meiobenthos actively leave the
sediment?
Copepoda, Ostracoda and Plathelminthes left the
sediment in significant numbers in all 3 trials of Expt I.
The number of emigrating Polychaeta was significantly
different from zero only in the continuously dark and
the day/night-rhythm trials. No significant emigration
was found in Nematoda and Oligochaeta in either case,
although they are major components of the benthos at
the sampled site. Veliger-larvae of Littorina littorea L.
and juvenile Bivalvia (mainly Cerstoderrna edule [L.])
also emigrated from the sediment. Veliger-larvae
behaved similarly to Copepoda and juvenile Bivalvia
behaved like Ostracoda. Both groups are however not
mentioned further.
Sorting of the sediment after 4 d of submersion was
performed on all 50 samples of Expts Ib and on 10
randomly chosen samples of Expts Ia and Ic. The
corresponding numbers of animals that remained in the
sediment allow for a n estimate of the percentage of
emigrated specimens (Table 1). Though the 3 trials
were not simultaneously performed and are thus not
adequate to test for the influence of light, the percentages indicate higher activity during darkness. This is
also seen in the periodical increase of emigrating
benthos in Expt Ic (Fig. 1). Significantly more specimens emigrated in the dark period than in the light.
However, such a pattern might also b e caused by an
endogenous diurnal rhythm.
Since the number of emigrating benthos seems to be
increased by continuous darkness and decreased by
continuous light, Expt Ic with a n 18/6 h day/night
rhythm is most appropriate to judge on the mobility of
benthos (Table 1). T h e percentage of Copepoda leaving the sediment during the first days, however, is too
Mar. Ecol. Prog. Ser. 43: 151-159, 1988
154
Table 1. Abundance of emigrated fauna in Expts Ia (1, light), Ib (d, darkness) and Ic (yd. lighwdarkness), and average number of
specimens that remained in the sediment. Total: sum of emigrated fauna (within 96 h) and fauna that remained in the sediment. X:
mean; SD: standard deviation; % , percentage of totals
Taxon
Emigrated
Withn 24 h
Copepoda
Ostracoda
Polychaeta
-
Remained
in sediment
X
R
R
SD
O/o
R
1
d
I/d
19.8
305.5
601.9
4.0
58.6
95.4
11.8
95.9
46.1
57.5
318.1
1200.7
11.6
65.8
152.4
34.4
99.8
92.0
167.3
318.7
1305.3
109.8
0.6
104.6
1
Vd
3.2
125.1
116.0
2.4
30.1
17.9
3.1
65.4
58.8
10.0
169.1
177.6
3.4
40.4
32.2
9.6
88.4
90.0
104.0
191.2
197.2
94.0
22.1
19.6
1
5.1
d
l/d
7.2
3.5
2.4
4.5
1.8
3.0
34.8
7.2
17 7
12.3
16.2
5.7
5.0
4.9
10.4
59.4
33.3
169.8
20.7
48.6
152.1
8.4
32.4
1
d
l/d
0.2
1.9
0.6
0.3
1.9
0.7
0.2
3.1
1.0
0.4
8.7
2.2
0.7
4.3
1.8
0.4
14.1
3.4
92.9
61.9
63.9
92.5
53.2
61.7
d
Plathelminthes
Total
Within 96 h
SD
Fig. 1. Course of emigration during 4 d of submergence (Expt
Ic, 18/6 h Light/dark cycle). Percentages of the totally emlgrated number of indviduals per taxon. Arrows indicate a
significant hfference between succeeding periods (U-test,
~ ~ 0 . 0 5 Decrease
).
in numbers over time results from the
emptying of sediment cores through emigration. Black and
white fields below columns indicate darkness and light, respectively
?o'
taxonomic composition of emigrated fauna is different
from that of fauna remaining in the sediment (significant differences in the rank order of abundance; Fig. 2).
From Expt I, the following conclusions can be derived:
(1) For the taxa Copepoda, Ostracoda, Plathelminthes
and Polychaeta, H, (1) is rejected. Members of these
taxa actively emigrated from the sediment.
(2) In the case of Copepoda, Ostracoda and Plathelminthes, emigration shows a marked periodicity coinciding with and possibly caused by differences in the
light regime. H, (2) should therefore be rejected. However, based on the number of animals that stayed in the
sediment up to a distinct point in time, the percentages
of Ostracoda and Copepoda leaving the sediment per
day do not significantly differ. In retrospect it seems a
fairly constant percentage of copepods left the sediment per day, causing a continuous decrease in numbers. With regard to the percentage emigration, H, (2),
hypothesising no differences in emigration among the
4 d, is accepted.
(3) H, (3) is rejected. The percentage taxonomic composition in the sediment significantly differs from that
of the emigrated fauna.
Experiment 11: Percentage emigration during one
tidal cycle of submersion
small because of high numbers of nauphus-larvae (not
included) and copepodites (included in copepods) in
the sediment. Development of nauplius-larvae to
copepodites increased the emigration rates of the final
days and the totals.
Since Nematoda and Oligochaeta remained in the
sediment while other taxa at least partly emigrated, the
Altogether 87 % of Copepoda, 67 % of Ostracoda,
and 42 O/O of Plathelminthes left the sediment during a
single simulated nocturnal high tide. The respective
percentages were considerably smaller during a diurnal high tide (Fig. 3). All percentages shouId be
regarded as minimum values: possibly some specimens
Armonies: Emergence of meiofauna from sediment
c
EMIGRATED
FAUNA
1
2
Fig. 2. Changes in the rank order of taxa between the fauna of original sediment (not submerged but sorted immediately), emigrated fauna, and the fauna remaining in the sediment
after 4 d of submersion (Expt Ib). Ranks are
based on significant differences in abundance
(U-test)
darkness
tr,
,
N = 6, 0 6
40
20
0
0
1
2
3h6
l
3
REMAINED I N
THE SEDIMENT
Nemotodo
1
Copepodo
2
P01
3
Ost
4.5
Oli
4
5.5
Nem
Oligochoeto
5.5
Oli
Plothelminthes
c0pepxi6;;
Nem
4.5
Plo
6
Cop
light
currents. During slack tides, there are periods of similar
length without strong currents in the field, and corresponding emergence of these taxa is expected. H, (4),
hypothesising a random pattern of emigration over 6 h,
is rejected.
A
m
S
Ostracoda
N . 148
ORIGINAL
SEDIMENT
N = 138
n
Plathelminlhes
Fig. 3. Course of emigration during 6 h of submersion (Expt 11).
Percentages of total abundance (N; ind. l ~ c m - ~S:
) . percentage remaining in the sediment. Because of low abundance the
p e r ~ o d3 to 6 h is combined. Arrows indicate s~gnificantdifference between successive penods
emerged from the sediment but returned prior to
sampling. Calculating from the base areas of the glass
jars (2.5 cm2) and aquaria (50 cm2),the probability of a
swimming animal returning accidentally to the inner
glass jars with sediment is about 5 %. Since the natural
sediment might be more attractive than a bare plastic
ground, the degree of underestimation may even be
higher than 5 %.
Copepoda and Plathelminthes show maximum emigration rates during the first hour of submersion (Fig.
3). Ostracods need more time to climb out of the glass
jars. This might either indicate a true delay in their
activity, or might be an artifact of the unnatural glass
container. However, in all cases considerable numbers
of animals emerge during l h of submergence without
Experiment 111: Distance meiobenthos swims above
the bottom
Although Ostracoda were highly active under comparable conditions in Expts I and I1 they were only once
found in a submerged box. There is no hint that
Ostracoda are able to swim actively. Among the active
swimmers, only Copepoda and Plathelminthes were in
sufficient numbers for a statistical evaluation. Abundance of Copepoda did not significantly differ between
the boxes fixed between 10 and 50 cm above ground
(Fig. 4). In the case of Plathelminthes the uppermost
box contained fewer individuals, which is significant
on a 5 % level, but not significant when p is adjusted to
an adequate level for 10-fold multiple comparisons.
There was no difference between the other heights.
Thus, concerning Copepoda and Plathelminthes, H, (5)
is maintained.
Experiment IV: Specific composition of emigrating
and non-emigrating Plathelminthes and Polychaeta
In Expt Ib, sediment samples were submerged and
significant numbers of Plathelminthes swam out into
the water column. After 4 d , all samples were sorted for
the benthos that remained in the sediment. Comparing
the numbers of emigrators versus non-emigrators, significant differences appear between taxa as well as
trophic groups (Table 2). Significantly more Proseriata,
Typhloplanoida and Dalyellioida emerged from the
sediment while more Kalyptorhynchia rested in the
sediment. On the species level, Promesostoma meixnen Ax, 1951, Pogaina suecica (Luther, 1948), Provor-
Mar. Ecol. Prog. Ser 4 3 : 151-159, 1988
156
E
from the sediment, and copepod-feedi.ng Plathelminthes did the same. Correspondingly, no nematode
emigration was observed, and most of the nematodefeeding Plathelminthes stayed in the sediment just as
did bacteria-feeders. Diatom-feeders and unspecific
predators on meiofauna and microfauna preferred to
leave the sediment.
Because of low abundance, no significant correlations were found between polychaete emergence and
their feeding-types. However, there were specific
differences in the emigration rates. Juvenile (mostly
< l cm long) Nereis diversicolor 0. F . Muller emigrated in the highest percentage, followed by Eteone
longa (Fabricius). Anaitides mucosa (Oersted) and
Pygospio elegans Claparede were already scarce and
others, such as Scoloplos armiger ( 0 .F . Muller), which
is the dominant polychaete at the investigated site,
were never found in the water column.
: Plathelrninthes
,;
Fig. 4 . Distribution of Copepoda and Plathelminthes over
boxes submerged in barrels (percentages per height, standard
deviation; Expt 111). Dotted line: 20% level expected in the
case of completely regular distribution over the entire range
DISCUSSION
Behavioral versus physically forced emergence
tex tubiferus Luther, 1948, Provortex psammophilus
Ax, 1951 and Cheliplanilla caudata Meixner, 1938 all
emigrated in significant numbers. Bresslauilla relicta
Reisinger, 1929 and Neoschizorhynchusparvorostro Ax
& Heller, 1970 on the other hand, preferred to remain in
the sediment during the 4 d of submersion.
Much of this variability is explained by the type of
feeding (Table 2). The majority of copepods emigrated
This study revealed 2 causal factors urging benthos
to enter the water column: (1) Most of the emerged
harpacticoids and Plathelminthes left the sediment
immediately after submersion. Significant differences
in the course of emigration indicate that emergence is
not just a casual event in these taxa but seems to be
regular, possibly triggered by endogenous factors. (2)
Table 2. Plathelminth taxa that showed significant differences between abundance in water column (emigrators) and in sediment
(non-emigrators) after 4 d of submersion in the dark (Expt Ib). X:Average abundance per 10 cm2 of sediment surface; SD: standard
deviation; ', ' ', ' ' ' Significance level (U-test, p < 0.05, 0.01, 0.001 respectively). Non-significant comparisons are omitted. B, C,
D , N , P: feeding types (see below)
Taxon and feeding types
Emigrators
X
Proseriata (P)
Typhloplanoida (mostly C)
Promesostoma meixnen (C)
Kalyptorhynchia (B and N]
Chehplanilla caudata (N)
Neoschizorhynchus parvorostro (B)
Dalyellioida (D, B and P)
Pogaina suecica (D)
Bressla uilla relicfa (B)
Provortex tubiferus (D)
Provortex psarnmophilus (P)
Feeding types:
D Diatom-feeders
B Bacteria-feeders
C Copepod-feeders
N Nematode-feeders
P Unspecific predators
SD
X
Non-emigrators
SD
Armonies: Emergence of meiofauna from sediment
In the polychaete Pygospio elegans emigration occurred only after l d of submersion and was possibly
caused by deterioration of environmental factors. This
might also be the cause for the significantly higher
number of Plathelminthes that left the glass jars after
the sediment had been turned upside down. Further
deterioration of physical factors such as oxygen content
in experiments longer than 4 d might lead to emergence of additional taxa (cf. Lorenzen et al. 1987).
The rapid emigration during the first 1 to 2 h of
experimental submersion in Copepoda, Plathelminthes
and Ostracoda indicates that deterioration of physical
factors is not the cause for their emergence - or else the
physical factors had already been extremely unfavourable in the field. However, as indicated by the effect of
light (Fig. l ) ,physical factors such as the light regime,
oxygen availability, and salinity do influence emigration rates (Armonies unpubl.), and biotic factors might
similarly be involved.
The 'laboratory environment' may be another factor
influencing emigration rates. Although the effects of
mechanical destruction of the sediment structure do
not indicate that the sampling procedure was harmful,
there is so far no adequate test for other factors.
All of the experiments described above were performed in the absence of flow. However, flow as well as
other hydrodynamic factors like hydrostatic pressure
may strongly influence the behavior of meiobenthos
(e. g. Boaden 1968, Fegley 1987). Therefore further
experiments were conducted to test for differences in
the emigrative behavior in gradients of physical factors
such as temperature, salinity and flow (Armonies
unpubl.). Results indicate that emergence is not an
artifact of the no-flow conditions, although the emergence pattern is indeed influenced by flow.
As a result of varying degrees of environmental
harshness and specific differences in the tendency to
leave the sediment, a regular gradient is expected
between plankton occasionally touching the sediment
and benthos occasionally emerging from the sediment.
On such a scale, Nematoda are relatively benthic and
most Copepoda are relatively planktonic. However,
this classification only meets the situation in the
studied intertidal sand flat. On more exposed beaches
epibenthic harpacticoids become rare (Mielke pers.
comm.),and interstitial species might be more benthic.
The fauna of muddy sites, on the other hand, seems to
include some good as well as bad swimmers (Palmer
1984).
In Plathelminthes and Polychaeta it seems that the
emergence rates can roughly be estimated by the
swimming ability of the respective species (observation
of the swimming ability in Petri dishes after mechanical
stimulation). Some differences also exist in copepods:
the slender interstitial species tend to emigrate less
157
rapidly than do the more voluminous epibenthic harpacticoids. Bell et al. (1987) reported on significant
correlations between morphological indices and the
habitat utilization and type of movement in seagrass
harpacticoids.
Consequences of emigration on distributional
patterns
As a consequence of active emigration from the sediment, short-term temporal variations in abundance and
population structure are expected, and for harpacticoids have already been demonstrated by Kern & Bell
(1984).Specific differences in the tendency to leave the
sediment (as demonstrated in Polychaeta and Plathelrninthes) may also cause short-term changes in the
fauna1 composition. Tischler (1979, p. 125) proposed
differentiating any list of species obtained from a single
habitat according to categories such as 'indigenous
species', 'visitors', and 'guests'. In the light of high
meiobenthic mobility, this suggestion seems also to be
appropriate for meiobenthic organisms, especially in
community studies and environmental monitoring.
Potential benefits versus potential risk of emersion
In Expt I1 (6 h submersion in the dark) an average of
48 copepods emigrated per 1 cm2 of sediment surface
during the first hour of submersion (Fig. 2). Since the
period of swimming activity of a single specimen is not
known, the actual abundance of benthos in the water
column can only be estimated: provided a single specimen swims no longer than 5 min, up to 40 000
copepods mP2 are simultaneously active in the water
column. Likewise, if the swimming period is only 1 min
8000 harpacticoids above 1 m2 of sediment surface
should be attractive enough to be a remunerative
source of food, e. g , for juvenile fish (Alheit & Scheibel
1982, Pihl & Rosenberg 1984, Pihl 1985). Small sizeclasses of the goby Poma toschistus minutus (Pallas)
even seem to prefer benthic harpacticoids to planktonic
calanoids (Zander & Hagemann 1987). Possibly the
benthic harpacticoids are easier to catch than
calanoids. The higher nocturnal than diurnal swimming activity may be useful in avoiding visual predators (Hobson & Chess 1976, Greening & Livingston
1982, Ohlhorst 1982, Fancett & l m m e r e r 1985) and the
joint emergence of many specimens during a restricted
period may be another way to reduce each individual's
risk of being preyed upon.
Additional prey (Decho 1986) and the possibility of
dispersal are advantages of emergence. Species with a
high rate of emersion might additionally increase their
Mar. Ecol. Prog. Ser. 43: 151-159, 1988
158
abundances from a small-scale towards a larger-scale
carrying capacity and thus more intensively exploit
resources (see Thistle 1980). Possibly emergence can
also help to escape predation within the sediment. The
high rates of emergence, despite the risk of being
preyed upon, indicate alone that there must be a net
advantage in regularly leaving the sediment, o r , at
least, no disadvantage.
Emergence increases the stability of the benthic
system
From an ecosystem point of view, emergence from
the sediment is regarded as an efficient way of energy
exchange between the benthos and pelagial. A high
abundance of food items in the water column can be
transferred to the benthos even before being
sedimented and an exceptionally high abundance of
swimming benthos will presumably increase the rate of
predation by pelagic predators. Small-scale disturbances of the benthic system may likewise be rapidly
compensated for (e. g. Sherman & Coull 1980, Thistle
1980, Hockin & Ollason 1981, Palmer & Brandt 1981,
Chandler & Fleeger 1983). Thus, high mobility may
increase the persistence of the benthic system and its
ability to absorb changes and disturbance and still
maintain the same relationships between species or
state variables (= resilience; Holling 1973).
Acknowledqernents. Expt I could not have been carried out
without the help of Monika Hellwig-Armonies. Karsten Reise
improved the manuscript by critical comments. This study was
supported by a grant of the Biologische Anstalt Helgoland.
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This article was submitted to the editor; it was accepted for printing on January 8, 1988